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ExperimentalModels of Cerebral Malaria

  • C. Engwerda
  • E. Belnoue
  • A. C. Grüner
  • L. Rénia
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 297)

Abstract

Malaria remains a major global health problem and cerebral malaria is one of themost serious complications of this disease. Recent years have seen important advances in our understanding of the pathogenesis of cerebralmalaria. Extensive analysis of tissues and blood taken frompatients with cerebralmalaria has been complimented by the use of animal models to identify specific components of pathogenic pathways. In particular, an important role for CD8+ T cells has been uncovered, as well divergent roles for members of the tumor necrosis factor (TNF) family of molecules, including TNF and lymphotoxin alpha. It has become apparent that theremay bemore than one pathogenic pathway leading to cerebral malaria. The last few years have also seen the testing of vaccines designed to target malaria molecules that stimulate inflammatory responses and thereby prevent the development of cerebral malaria. In this review, we will discuss the above advancements, as well as other important findings in research into the pathogenesis of cerebral malaria. As our understanding of pathogenic responses to Plasmodium parasites gathers momentum, the chance of a breakthrough in the development of treatments and vaccines to prevent death fromcerebralmalaria have become more realistic.

Keywords

Migration Inhibitory Factor Cerebral Malaria Plasmodium Falciparum Malaria Plasmodium Berghei Experimental Cerebral Malaria 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Adams S, Brown H, Turner GDH (2002) Breaking down the blood-brain barrier: signaling a path to cerebral malaria? Trends Parasitol 18:348–351CrossRefGoogle Scholar
  2. Alger NE (1963) Distribution of schizonts of Plasmodium berghei in tissues of rats, mice and hamsters. J Protozool 10:6–10PubMedGoogle Scholar
  3. Amani V, Boubou MI, Pied S, Marussig M, Walliker D, Mazier D, Rénia L (1998) Cloned lines of Plasmodium berghei ANKA differ in their abilities to induce experimental cerebral malaria1. Infect Immun 66:4093–4099PubMedGoogle Scholar
  4. Amani V, Vigario AM, Belnoue E, Marussig M, Fonseca L, Mazier D, Renia L (2000) Involvement of IFN-gamma receptor-medicated signaling in pathology and antimalarial immunity induced by Plasmodium berghei infection. Eur J Immunol 30:1646–1655PubMedCrossRefGoogle Scholar
  5. Andjelkovic AV, Pachter JS (2000) Characterization of binding sites for chemokines MCP-1 and MIP-1alpha on human brain microvessels. JNeurochem 75:1898–1906CrossRefGoogle Scholar
  6. Anstey NM, Weinberg JB, Hassanali MY, Mwaikambo ED, Manyenga D, Misukonis MA, Arnelle DR, Hollis D, McDonald MI, Granger DL (1996) Nitric oxide in Tanzanian children with malaria: inverse relationship between malaria severity and nitric oxide production/nitric oxide synthase type 2 expression. J Exp Med 184:557–567PubMedCrossRefGoogle Scholar
  7. Artavanis-Tsakonas K, Riley EM (2002) Innate immune response to malaria: rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes. J Immunol 169:2956–2963PubMedGoogle Scholar
  8. Artavanis-Tsakonas K, Eleme K, McQueen KL, Cheng NW, Parham P, Davis DM, Riley EM (2003) Activation of a subset of human NK Cells upon contact with Plasmodium falciparum-infected erythrocytes. J Immunol 171:5396–5405PubMedGoogle Scholar
  9. Bafort JM, Pryor WH, Ramsey JM(1980) Immunization of rats against malaria: a new model. J Parasitol 66:337–338PubMedGoogle Scholar
  10. Bagot S, Idrissa-Boubou M, Campino S, Behrschmidt C, Gorgette O, Guénet JL, Penha-Gonçalves C, Mazier D, Pied S, Cazenave PA (2002) Susceptibility to experimental cerebral malaria induced by Plasmodium berghei ANKA in inbred mouse strains recently derived from wild stock. Infect Immun 70:2049–2056PubMedCrossRefGoogle Scholar
  11. Bagot S, Nogueira F, Collette A, do Rosario VE, Lemonier F, Cazenave PA, Pied S (2004) Comparative Study of Brain CD8(+) T cells induced by sporozoites and those induced by blood-stage Plasmodium berghei ANKA involved in the development of cerebral malaria. Infect Immun 72:2817–2826PubMedCrossRefGoogle Scholar
  12. Bakker NPM, Eling WMC, De Groot AMTh, Sinkeldam EJ, Luyken R(1992) Attenuation of malaria infection, paralysis and lesions in the central nervous system by low protein diets in rats. Acta Trop 50:285–293PubMedGoogle Scholar
  13. Ball HJ, MacDougall HG, McGregor IS, Hunt NH (2004) Cyclooxygenase-2 in the Pathogenesis of Murine Cerebral Malaria. J Infect Dis 189:751–758PubMedCrossRefGoogle Scholar
  14. Belnoue E, Kayibanda M, Vigario AM, Deschemin JC, van Rooijen N, Viguier M, Snounou G, Rénia L (2002) On the pathogenic role of brain-sequestered αβ CD8+ T cells in experimental cerebral malaria. J Immunol 169:6369–6375PubMedGoogle Scholar
  15. Belnoue E, Costa FTM, Vigario AM, Voza T, Gonnet F, Landau I, van Rooijen N, Mack M, Kuziel WA, Rénia L (2003) Chemokine receptor CCR2 is not essential for the development of experimental cerebral malaria. Infect Immun 71:3648–3651PubMedCrossRefGoogle Scholar
  16. Belnoue E, Kayibanda M, Deschemin JC, Viguier M, Mack M, Kuziel WA, Rénia L (2003) CCR5 deficiency decreases susceptibility to experimental cerebral malaria. Blood 101:4253–4259PubMedCrossRefGoogle Scholar
  17. Berendt AR, Turner GDH, Newbold CI (1994) Cerebral malaria: the sequestration hypothesis. Parasitol Today 10:412–414PubMedCrossRefGoogle Scholar
  18. Bondi FS (1992) The incidence and outcome of neurological abnormalities in childhood cerebral malaria: a long-term follow-up of 62 survivors. Trans R Soc Trop Med Hyg 86:17–19PubMedCrossRefGoogle Scholar
  19. Boubou MI, Collette A, Voegtle D, Mazier D, Cazenave PA, Pied S (1999) T cell response in malaria pathogenesis: selective increase in T cells carrying the TCR V(beta)8 during experimental cerebral malaria. Int Immunol 11:1553–1562PubMedCrossRefGoogle Scholar
  20. Boutlis CS, Tjitra E, Maniboey H, Misukonis MA, Saunders JR, Suprianto S, Weinberg JB, Anstey NM (2003) Nitric oxide production and mononuclear cell nitric oxide synthase activity in malaria-tolerant Papuan adults. Infect Immun 71:3682–3689PubMedGoogle Scholar
  21. Brewster DR, Kwiatkowski DP, White NJ (1990) Neurological Sequelae of Cerebral Malaria in Children. Lancet 336:1039–1043PubMedCrossRefGoogle Scholar
  22. Brown H, Turner G, Rogerson S, Tembo M, Mwenechanya J, Molyneux M, Taylor T (1999) Cytokine expression in the brain in human cerebral malaria. J Infect Dis 180: 1742–1746PubMedGoogle Scholar
  23. Calandra T, Bucala R (1997) Macrophage migration inhibitory factor (MIF): a glucocorticoid counter-regulator within the immune system. Crit Rev Immunol 17:77–88PubMedGoogle Scholar
  24. Carvalho LH, Sano G, Hafalla JC, Morrot A, Curotto de Lafaille MA, Zavala F (2002) IL-4-secreting CD4+ T cells are crucial to the development of CD8+ T-cell responses against malaria liver stages. Nature Med 8:166–170PubMedGoogle Scholar
  25. Chang WL, Jones SP, Lefer DJ, Welbourne T, Sun G, Yin L, Suzuki H, Huang J, Granger DN, van der Heyde HC (2001) CD8+-T-Cell Depletion Ameliorates Circulatory Shock in Plasmodium berghei-Infected Mice. Infect Immun 69:7341–7348PubMedCrossRefGoogle Scholar
  26. Chen Q, Barragan A, Fernandez V, Sundstrom A, Schlichtherle M, Sahlen A, Carlson J, Datta S, Wahlgren M (1998) Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J Exp Med 187:15–23PubMedCrossRefGoogle Scholar
  27. Chen L, Zhang Z, Sendo F (2000) Neutrophils play a critical role in the pathogenesis of experimental cerebral malaria. Clin Exp Immunol 120:125–133PubMedCrossRefGoogle Scholar
  28. Chen L, Sendo F (2001) Cytokine and chemokine mRNA expression in neutrophils from CBA/NSlc mice infected with Plasmodium berghei ANKA that induces experimental cerebral malaria. Parasitol Int 50:139–143PubMedGoogle Scholar
  29. Clark IA, Virelizier JL, Carswell EA, Wood PR (1981) Possible importance of macrophage-derived mediators in acute malaria. Infect Immun 32:1058–1066PubMedGoogle Scholar
  30. Clark IA, Rockett KA, Cowden WB (1991) Proposed link between cytokines, nitric oxide and human cerebral malaria. Parasitol Today 7:205–207PubMedCrossRefGoogle Scholar
  31. Clark IA, Awburn MM, Whitten RO, Harper CG, Liomba NG, Molyneux ME, Taylor TE (2003) Tissue distribution of migration inhibitory factor and inducible nitric oxide synthase in falciparum malaria and sepsis in African children. Malar J 2:6PubMedGoogle Scholar
  32. Clark IA, Cowden WB (2003) The pathophysiology of falciparum malaria. Pharmacol Ther 99:221–260PubMedCrossRefGoogle Scholar
  33. Clark IA, Alleva LM, Mills AC, Cowden WB (2004) Pathogenesis of malaria and clinically similar conditions. Clin Microbiol Rev 17:509–539PubMedCrossRefGoogle Scholar
  34. Combes V, Rosenkranz AR, Redard M, Pizzolato G, Lepidi H, Vestweber D, Mayadas TN, Grau GE (2004) Pathogenic role of P-selectin in experimental cerebral malaria: importance of the endothelial compartment. Am J Pathol 164:781–786PubMedGoogle Scholar
  35. Coquelin F, Boulard Y, Mora-Silvera E, Richard F, Chabaud AG, Landau I (1999) Final stage of maturation of the erythrocytic schizonts of rodent Plasmodium in the lungs 9075. C R Acad Sci (III) 322:55–62Google Scholar
  36. Cordeiro RSB, Cunha FQ, Filho JA, Flores CA, Vasconcelos HN, Martins MA (1983) Plasmodium berghei: physiopathological changes during infections in mice. Ann Trop Med Parasitol 77:455–465PubMedGoogle Scholar
  37. Cox J, Semoff S, Hommel M (1987) Plasmodium chabaudi: a rodent malaria model for in vivo and in vitro cytoadherence of malaria parasites in the absence of knobs. Parasite Immunol 9:543–561PubMedGoogle Scholar
  38. Craig A, Scherf A (2001) Molecules on the surface of the Plasmodium falciparum infected erythrocyte and their role in malaria pathogenesis and immune evasion. Mol Biochem Parasitol 115:129–143PubMedCrossRefGoogle Scholar
  39. Curfs JHAJ, van Der Meer JWM, Sauerwein RW, Eling WMC (1990) IL-1 treatment inhibits parasitemia and protects against development of cerebral hemorrhages in Plasmodium berghei infected mice. The physiological and pathological effects of cytokines. Wiley-Liss, Inc., pp 331–337Google Scholar
  40. Day NP, Hien TT, Schollaardt T, Loc PP, Chuong LV, Chau TT, Mai NT, Phu NH, Sinh DX, White NJ, Ho M (1999) The prognostic and pathophysiologic role of pro-and antiinflammatory cytokines in severe malaria. J Infect Dis 180:1288–1297PubMedCrossRefGoogle Scholar
  41. De Kossodo S, Grau GE (1993) Role of cytokines and adhesion molecules in malaria immunopathology. Stem Cells 11:41–48PubMedGoogle Scholar
  42. De Kossodo S, Monso C, Juillard P, Velu T, Goldman M, Grau GE (1997) Interleukin-10 modulates susceptibility in experimental cerebral malaria. Immunology 91:536–540PubMedCrossRefGoogle Scholar
  43. De Souza JB, Riley EM (2002) Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis.Microbes Infect 4:291–300PubMedGoogle Scholar
  44. Dean M, Carrington M, O’Brien SJ (2002) Balanced polymorphism selected by genetic versus infectious human disease. Annu Rev Genomics Hum Genet 3:263–292PubMedCrossRefGoogle Scholar
  45. Deininger MH, Kremsner PG, Meyermann R, Schluesener HJ (2000) Differential cellular accumulation of transforming growth factor-beta1,-beta2, and-beta3 in brains of patients who died with cerebral malaria. J Infect Dis 181:2111–2115PubMedGoogle Scholar
  46. Dennis LH, Eichelberger JW, Jr., Inman MM, Conrad ME (1967) Depletion of coagulation factors in drug-resistant Plasmodium falciparum malaria. Blood 29: 713–721PubMedGoogle Scholar
  47. Desowitz RS, Barnwell JW (1976) Plasmodium berghei: deep vascular sequestration of young forms in the heart and kidney of the white rat. Ann Trop Med Parasitol 70:475–476PubMedGoogle Scholar
  48. Devakul K, Harinasuta T, Reid HA (1966) 125I-labelled fibrinogen in cerebral malaria. Lancet 288:886–888CrossRefGoogle Scholar
  49. Di Perri G, Di Perri IG, Monteiro GB, Bonora S, Hennig C, Cassatella M, Micciolo R, Vento S, Dusi S, Bassetti D. (1995) Pentoxifylline as a supportive agent in the treatment of cerebral malaria in children. J Infect Dis 171:1317–1322PubMedGoogle Scholar
  50. Dietrich JB (2002) The adhesion molecule ICAM-1 and its regulation in relation with the blood-brain barrier. J Neuroimmunol 128:58–68PubMedCrossRefGoogle Scholar
  51. Dorner BG, Scheffold A, Rolph MS, Huser MB, Kaufmann SHE, Radbruch A, Flesch IEA, Kroczek RA (2002) MIP-1α, MIP-1β, RANTES, and ATAC/lymphotactin function together with IFN-γ as type 1 cytokines. Proc Natl Acad Sci U S A 99:6181–6186PubMedCrossRefGoogle Scholar
  52. Durck H (1917) Uber die bei malaria comatosa aufretenden veranderungen des zentralnervensystems. Arch Schiff Tropenhygien 21:117–132Google Scholar
  53. Eckwalanga M, Marussig M, Tavares MD, Bouanga JC, Hulier E, Pavlovitch JH, Minoprio P, Portnoi D, Rénia L, Mazier D (1994) Murine AIDS protects mice against experimental cerebral malaria: Down-regulation by interleukin 10 of a T-helper type 1 CD4+ cell-mediated pathology. Proc Natl Acad Sci USA 91:8097–8101PubMedGoogle Scholar
  54. Edington GM (1967) Pathology of malaria in West Africa. Br Med J 1:715–718PubMedCrossRefGoogle Scholar
  55. Engwerda CR, Mynott TL, Sawhney S, De Souza JB, Bickle QD, Kaye PM (2002) Locally up-regulated lymphotoxin alpha, not systemic tumor necrosis factor alpha, is the principle mediator of murine cerebral malaria. J Exp Med 195:1371–1377PubMedCrossRefGoogle Scholar
  56. Falanga PB, Butcher EC (1991) Late treatment with anti-LFA-1 (CD11a) antibody prevents cerebral malaria in a mouse model. Eur J Immunol21:2259–2263PubMedGoogle Scholar
  57. Favre N, Da Laperousaz C, Ryffel B, Weiss NA, Imhof BA, Rudin W, Lucas R, Piguet PF (1999) Role of ICAM-1 (CD54) in the development of murine cerebral malaria. Microbes Infect 1:961–968PubMedCrossRefGoogle Scholar
  58. Favre N, Ryffel B, Rudin W (1999) The development of murine cerebral malaria does not require nitric oxide production. Parasitology 118:135–138PubMedGoogle Scholar
  59. Fife BT, Huffnagle GB, Kuziel WA, Karpus WJ (2000) CC chemokine receptor 2 is critical for induction of experimental autoimmune encephalomyelitis. J Exp Med 192:899–905PubMedGoogle Scholar
  60. Finley RW, Mackey LJ, Lambert PH (1982) Virulent P. berghei malaria: prolonged survival and decreased cerebral pathology in cell-dependent nude mice. J Immunol 129:2213–2218PubMedGoogle Scholar
  61. Franz DR, Lee M, Seng LT, Young GD, Baze WB, Lewis GEJ (1987) Peripheral vascular pathophysiology of Plasmodium berghei infection: a comparative study in the cheek pouch and brain of the golden hamster. Am J Trop Med Hyg 36:474–480PubMedGoogle Scholar
  62. Gaskell SJ, Millar WL (1920) Studies on malignant malaria in Macedonia. Q J Med 24:317–322Google Scholar
  63. Gear AR, Camerini D (2003) Platelet chemokines and chemokine receptors: linking hemostasis, inflammation, and host defense. Microcirculation 10:335–350PubMedCrossRefGoogle Scholar
  64. Gilks CF, Walliker D, Newbold CI (1990) Relationships between sequestration, antigenic variation and chronic parasitism in Plasmodium chabaudi chabaudi-a rodent malaria model. Parasite Immunol 12:45–64PubMedGoogle Scholar
  65. Gimenez F, Barraud de Lagerie S, Fernandez C, Pino P, Mazier D (2003) Tumor necrosis factor alpha in the pathogenesis of cerebral malaria. Cell Mol Life Sci 60:1623–1635PubMedCrossRefGoogle Scholar
  66. Goodier MR, Lundqvist C, Hammarstrom ML, Troye-Blomberg M, Langhorne J (1995) Cytokine profiles for human V gamma 9+ T cells stimulated by Plasmodium falciparum. Parasite Immunol 17:413–423PubMedGoogle Scholar
  67. Gorgette O, Existe A, Boubou MI, Bagot S, Guenet JL, Mazier D, Cazenave PA, Pied S (2002) Deletion of T cells bearing the Vβ8.1T-cell receptor following mouse mammary tumor virus 7 integration confers resistance to murine cerebral malaria. Infect Immun 70:3701–3706PubMedCrossRefGoogle Scholar
  68. Grau GE, Piguet PF, Engers HD, Louis JA, Vassalli P, Lambert PH (1986) L3T4+ T lymphocytes play a major role in the pathogenesis of murine cerebral malaria. J Immunol 137:2348–2354PubMedGoogle Scholar
  69. Grau GE, Del Giudice G, Lambert PH (1987a) Host immune response and pathological expression in malaria: possible implications for malaria vaccines. Parasitology 94:123–137Google Scholar
  70. Grau GE, Fajardo LF, Piguet PF, Allet B, Lambert PH, Vassalli P (1987b) Tumor necrosis factor (cachectin) as an essential mediator in murine cerebral malaria. Science 237:1210–1212PubMedGoogle Scholar
  71. Grau GE, Piguet PF, Gretener D, Vesin C, Lambert PH (1988) Immunopathology of thrombocytopenia in experimental malaria. Immunology 65:501–506PubMedGoogle Scholar
  72. Grau GE, Heremans H, Piguet PF, Pointaire P, Lambert PH, Billiau A, Vassalli P (1989a) Monoclonal antibody against interferon gamma can prevent experimental cerebral malaria and its associated overproduction of tumor necrosis factor. Proc Natl Acad Sci USA 86:5572–5574PubMedGoogle Scholar
  73. Grau GE, Taylor TE, Molyneux ME, Wirima JJ, Vassalli P, Hommel M, Lambert PH (1989b) Tumor necrosis factor and disease severity in children with falciparum malaria. N Engl J Med 320:1586–1591PubMedCrossRefGoogle Scholar
  74. Grau GE, Bieler G, Pointaire P, De Kossodo S, Tacchini-Cottier F, Vassalli P, Piguet PF, Lambert PH (1990a) Significance of cytokine production and adhesion molecules in malarial immunopathology. Immunol Lett 25:189–194PubMedCrossRefGoogle Scholar
  75. Grau GE (1990b) Implications of cytokines in immunopathology: experimental and clinical data. Eur Cyt Netw 1:203–210Google Scholar
  76. Grau GE, Pointaire P, Piguet PF, Vesin C, Rosen H, Stamenkovic I, Takei F, Vassalli P (1991) Late administration of monoclonal antibody to leukocyte function-antigen 1 abrogates incipient murine cerebral malaria. Eur J Immunol 21:2265–2267PubMedGoogle Scholar
  77. Grau GE, Tacchini-Cottier F, Vesin C, Milon G, Lou JN, Piguet PF, Juillard P (1993) TNF-induced microvascular pathology: active role for platelets and importance of the LFA-1/ICAM-1 interaction. Eur Cytokine Netw 4:415–419PubMedGoogle Scholar
  78. Grau GE, Mackenzie CD, Carr RA, Redard M, Pizzolato G, Allasia C, Cataldo C, Taylor TE, Molyneux ME (2003) Platelet accumulation in brain microvessels in fatal pediatric cerebral malaria. J Infect Dis 187:461–466PubMedCrossRefGoogle Scholar
  79. Gyan B, Troye-Blomberg M, Perlmann P, Bjorkman A (1994) Human monocytes cultured with and without interferon-gamma inhibit Plasmodium falciparum parasite growth in vitro via secretion of reactive nitrogen intermediates. Parasite Immunol 16:371–375PubMedGoogle Scholar
  80. Haas W, Pereira P, Tonegawa S (1993) γδ cells. Annu Rev Immunol 11: 637–685PubMedGoogle Scholar
  81. Hansen DS, Siomos MA, Buckingham L, Scalzo AA, Schofield L (2003) Regulation of murine cerebral malaria pathogenesis by CD1d-restricted NKT Cells and the natural killer complex. Immunity 18:391–402PubMedCrossRefGoogle Scholar
  82. Hanum PS, Hayano M, Kojima S (2003) Cytokine and chemokine responses in a cerebral malaria-susceptible or-resistant strain of mice to Plasmodium berghei ANKA infection: early chemokine expression in the brain. Int Immunol 15:633–640Google Scholar
  83. Haque A, Graille M, Kasper LH, Haque S (1999) Immunization with heat-killed Toxoplasma gondii stimulates an early IFN-gamma response and induces protection against virulent murine malaria. Vaccine 17:2604–2611PubMedCrossRefGoogle Scholar
  84. Hatabu T, Kawazu SI, Aikawa M, Kano S (2003) Binding of Plasmodium falciparum infected erythrocytes to the membrane-bound form of Fractalkine/CX3CL1. Proc Natl Acad Sci USA 100:15942–15946PubMedCrossRefGoogle Scholar
  85. Hearn J, Rayment N, Landon DN, Katz DR, De Souza JB (2000) Immunopathology of cerebral malaria: morphological evidence of parasite sequestration in murine brain microvasculature. Infect Immun 68:5364–5376PubMedCrossRefGoogle Scholar
  86. Heddini A (2002) Malaria pathogenesis: a jigsaw with an increasing number of pieces. Int J Parasitol 32:1587–1598PubMedGoogle Scholar
  87. Hensmann M, Kwiatkowski D (2001) Cellular basis of early cytokine response to Plasmodium falciparum. Infect Immun 69:2364–2371PubMedCrossRefGoogle Scholar
  88. Hermsen C, van de Wiel T, Mommers E, Sauerwein R, Eling WMC (1997a) Depletion of CD4+ or CD8+ T-cells prevents Plasmodium berghei induced cerebral malaria in end-stage disease. Parasitology 114:7–12PubMedCrossRefGoogle Scholar
  89. Hermsen CC, Crommert JVD, Fredrix H, Sauerwein RW, Eling WMC (1997b) Circulating tumour necrosis factor α is not involved in the development of cerebral malaria in Plasmodium berghei-infected C57BL mice. Parasite Immunol. 19:571–577PubMedCrossRefGoogle Scholar
  90. Hermsen CC, Mommers E, van de Wiel T, Sauerwein RW, Eling WM (1998) Convulsions due to increased permeability of the blood-brain barrier in experimental cerebral malaria can be prevented by splenectomy or anti-T cell treatment. J Infect Dis 178:1225–1227PubMedGoogle Scholar
  91. Ho M, Sexton MM, Tongtawe P, Looareesuwan S, Suntharasamai P, Webster HK (1995) Interleukin-10 inhibits tumor necrosis factor production but not antigenspecific lymphoproliferation in acute Plasmodium falciparum malaria. J Infect Dis 172:838–844PubMedGoogle Scholar
  92. Horstmann RD, Dietrich M, Bienzle U, Rasche H (1981) Malaria-induced thrombocytopenia. Blut 42:157–164PubMedCrossRefGoogle Scholar
  93. Huffnagle GB, McNeil LK, McDonald RA, Murphy JW, Toews GB, Maeda N, Kuziel WA (1999) Role of C-C Chemokine Receptor 5 in Organ-Specific and Innate Immunity to Cryptococcus neoformans. J Immunol 163:4642–4646PubMedGoogle Scholar
  94. Hunt NH, Driussi C, Sai-Kiang L (2002) Haptoglobin and malaria. Redox Rep 6: 389–392Google Scholar
  95. Hunt NH, Grau GE (2003) Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol. 24:491–499PubMedCrossRefGoogle Scholar
  96. Hviid L, Kurtzhals JAL, Adabayeri V, Loizon S, Kemp K, Goka BQ, Lim A, Mercereau-Puijalon O, Akanmori BD, Behr C (2001) Perturbation and Proinflammatory Type Activation of Vδ1(+) γδ T Cells in African Children with Plasmodium Falciparum Malaria. Infect Immun 69:3190–3196PubMedCrossRefGoogle Scholar
  97. Jacobs T, Graefe SE, Niknafs S, Gaworski I, Fleischer B (2002) Murine malaria is exacerbated by CTLA-4 blockade. J Immunol 169:2323–2329PubMedGoogle Scholar
  98. Jadin J, Timperman G, De Ruysser F (1975) Comportement d’une lignée de P. berghei après préservation à basse température pendant plus de dix ans. Ann Soc Belge Med Trop 55:603–608Google Scholar
  99. Jennings VM, Actor JK, Lal AA, Hunter RL (1997) Cytokine profile suggesting that murine cerebral malaria is an encephalitis. Infect Immun 65:4883–4887PubMedGoogle Scholar
  100. Kamiyama T, Tatsumi M, Matsubara J, Yamamoto K, Rubio Z, Cortes G, Fujii H (1987) Manifestation of cerebral malaria-like symptoms in the WM/Ms rat infected with Plasmodium berghei strain NK65. J Parasitol 73:1138–1145PubMedGoogle Scholar
  101. Kaul DK, Nagel RL, Llena JF, Shear HL (1994) Cerebral malaria in mice: demonstration of cytoadherence of infected red blood cells and microrheologic correlates. Am J Trop Med Hyg 50:512–521PubMedGoogle Scholar
  102. Kean BH, Smith JA (1944) Death due to estivo-autumnal malaria. A resumé of one hundred autopsy cases, 1925-1942. Am J Trop Med 24:317–322Google Scholar
  103. Kern P, Hemmer CJ, Van Damme J, Gruss HJ, Dietrich M (1989) Elevated tumor necrosis factor alpha and interleukin-6 serum levels as markers for complicated Plasmodium falciparum malaria. Am J Med 87:139–43PubMedCrossRefGoogle Scholar
  104. Koller BH, Marrack P, Kappler JW, Smithies O (1990) Normal development of mice deficient in β2 M, MHC class I proteins, and CD8+ T cells. Nature 248: 1227–1229Google Scholar
  105. Kremsner PG, Bienzle U (1989) Soluble CD8 antigen in Plasmodium falciparum malaria. J Infect Dis 160:357–358PubMedGoogle Scholar
  106. Kurtzhals JA, Adabayeri V, Goka BQ, Akanmori BD, Oliver-Commey JO, Nkrumah FK, Behr C, Hviid L (1998) Low plasma concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria. Lancet 351:1768–1772PubMedCrossRefGoogle Scholar
  107. Kuziel WA, Morgan SJ, Dawson TC, Griffin S, Smithies O, Ley K, Maeda N (1997) Severe reduction in leukocyte adhesion and monocyte extravasation in mice deficient in CC chemokine receptor 2. Proc Natl Acad Sci USA 94:12053–12058PubMedCrossRefGoogle Scholar
  108. Kuziel WA, Dawson TC, Quinones M, Garavito E, Chenaux G, Ahuja SS, Reddick RL, Maeda N (2003) CCR5 deficiency is not protective in the early stages of atherogenesis in apoE knockout mice. Atherosclerosis 167:25–32PubMedCrossRefGoogle Scholar
  109. Kwiatkowski D, Cannon JG, Manogue KR, Cerami A, Dinarello CA, Greenwood BM (1989) Tumour necrosis factor production in Falciparum malaria and its association with schizont rupture. Clin Exp Immunol 77:361–366PubMedGoogle Scholar
  110. Kwiatkowski D, Hill AV, Sambou I, Twumasi P, Castracane J, Manogue KR, Cerami A, Brewster DR, Greenwood BM (1990) TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336: 1201–1204PubMedCrossRefGoogle Scholar
  111. Landau I, Boulard Y (1978) Life cycles and morphology. In: Killick-Kendrick R, Peters W (eds) Rodent malaria. Academic Press, London, pp 53–84Google Scholar
  112. Lisbonne M, Leite de Moraes MC (2003) Invariant Vα14 NKT lymphocytes: a doubleedged immuno-regulatory T cell population. Eur Cyt Netw 14:4–14Google Scholar
  113. Lopansri BK, Anstey NM, Weinberg JB, Stoddard GJ, Hobbs MR, Levesque MC, Mwaikambo ED, Granger DL (2003) Low plasma arginine concentrations in children with cerebral malaria and decreased nitric oxide production. Lancet 361:676–678PubMedCrossRefGoogle Scholar
  114. Lou J, Donati YR, Juillard P, Giroud C, Vesin C, Mili N, Grau GE (1997) Platelets play an important role in TNF-induced microvascular endothelial cell pathology. Am J Pathol 151:1397–405PubMedGoogle Scholar
  115. Lou J, Lucas R, Grau GE (2001) Pathogenesis of cerebral malaria: recent experimental data and possible applications for humans. Clin Microbiol Rev 14:810–820PubMedCrossRefGoogle Scholar
  116. Lucas R, Juillard P, Decoster E, Redard M, Burger D, Donati Y, Giroud C, Monso-Hinard C, DeKesel T, Buurman WA, Moore MW, Dayer JM, Fiers W, Bluethmann H, Grau GE (1997) Crucial role of tumor necrosis factor (TNF) receptor 2 and membranebound TNF in experimental cerebral malaria. Eur J Immunol 27:1719–1725PubMedGoogle Scholar
  117. Mackey LJ, Hochmann A, June CH, Contreras CE, Lambert PH (1980) Immunopathological aspects of Plasmodium berghei infection in five strains of mice. II. Immunopathology of cerebral and other tissue lesions during the infection. Clin Exp Immunol 42:412–420PubMedGoogle Scholar
  118. MacMicking J, Xie QW, Nathan C (1997) Nitric oxide and macrophage function. Annu Rev Immunol 15:323–350PubMedCrossRefGoogle Scholar
  119. MacPherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA (1985) Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am J Pathol 119:385–401PubMedGoogle Scholar
  120. Maegraith BG, Fletcher A (1972) The pathogenesis of mammalian malaria. Adv Parasitol 10:49–72PubMedGoogle Scholar
  121. Maneerat Y, Viriyavejakul P, Punpoowong B, Jones M, Wilairatana P, Pongponratn E, Turner GD, Udomsangpetch R (2000) Inducible nitric oxide synthase expression is increased in the brain in fatal cerebral malaria. Histopathology 37:269–277PubMedCrossRefGoogle Scholar
  122. Marchiafava E, Bignami A (1900) Malaria. Twentieth century practice of Medicine. Sampson Lowe, LondonGoogle Scholar
  123. Margulis MS (1914) Zur frage der pathologish-anatomischen veränderungen bei bösartige malaria. Neurologishe Zentralblat 33:1019–1024Google Scholar
  124. May J, Lell B, Luty AJ, Meyer CG, Kremsner PG (2000) Plasma interleukin-10:Tumor necrosis factor (TNF)-alpha ratio is associated with TNF promoter variants and predicts malarial complications. J Infect Dis 182:1570–1573PubMedCrossRefGoogle Scholar
  125. Mercado TI (1965) Paralysis associated with Plasmodium berghei malaria in the rat13982. J Infect Dis 115:465–472PubMedGoogle Scholar
  126. Miller LH, Fremount HN (1969) The sites of deep vascular schizogony in chloroquine-resistant Plasmodium berghei in mice. Trans R Soc Trop Med Hyg 63:195–197PubMedCrossRefGoogle Scholar
  127. Monso-Hinard C, Lou JN, Behr C, Juillard P, Grau GE (1997) Expression of major histocompatibility complex antigens on mouse brain microvascular endothelial cells in relation to susceptibility to cerebral malaria. Immunology 92:53–59PubMedCrossRefGoogle Scholar
  128. Mota MM, Jarra W, Hirst E, Patnaik PK, Holder AA (2000) Plasmodium chabaudi-infected erythrocytes adhere to CD36 and bind to microvascular endothelial cells in an organ-specic way. Infect Immun 68:4135–4144PubMedCrossRefGoogle Scholar
  129. Neill AL, Hunt NH (1992) Pathology of fatal and resolving Plasmodium berghei cerebral malaria in mice. Parasitology 105:165–175PubMedGoogle Scholar
  130. Neill AL, Chan-Ling T, Hunt NH (1993) Comparisons between microvascular changes in cerebral and non-cerebral malaria in mice, using the retinal whole-mount technique. Parasitology 107:477–487PubMedCrossRefGoogle Scholar
  131. Nitcheu J, Bonduelle O, Combadiere C, Tefit M, Seilhean D, Mazier D, Combadiere B (2003) Perforin-dependent brain-infiltrating cytotoxic CD8(+) T lymphocytes mediate experimental cerebral malaria pathogenesis. J Immunol 170:2221–2228PubMedGoogle Scholar
  132. O’Brien SJ, Moore JP (2000) The effect of genetic variation in chemokines and their receptors on HIV transmission and progression to AIDS. Immunol Rev 177:99–111PubMedGoogle Scholar
  133. Pain A, Ferguson DJ, Kai O, Urban BC, Lowe B, Marsh K, Roberts DJ (2001) Platelet-mediated clumping of Plasmodium falciparum-infected erythrocytes is a common adhesive phenotype and is associated with severe malaria. Proc Natl Acad Sci USA 98:1805–1810PubMedCrossRefGoogle Scholar
  134. Patnaik JK, Das BS, Mishra SK, Mohanty S, Satpathy SK, Mohanty D (1994) Vascular clogging, mononuclear cell margination, and enhanced vascular permeability in the pathogenesis of human cerebral malaria. Am J Trop Med Hyg 51:642–647PubMedGoogle Scholar
  135. Perarnau B, Saron MF, San Martin BR, Bervas N, Ong HC, Soloski MJ, Smith AG, Ure JM Gairin JE, Lemonnier FA (1999) Single H2 K b, H2Db and double H2 KbDb knockout mice: peripheral CD8+ T cell repertoire and anti-lymphocytic choriomeningitis virus cytolytic responses. Eur J Immunol 29:1243–1252PubMedGoogle Scholar
  136. Piguet PF, Da Laperrousaz C, Vesin C, Tacchini-Cottier F, Senaldi G, Grau GE(2000) Delayed mortality and attenuated thrombocytopenia associated with severe malaria in urokinase-and urokinase receptor-deficient mice. Infect Immun 68:3822–3829PubMedCrossRefGoogle Scholar
  137. Piguet PF, Da Kan C, Vesin C, Rochat A, Donati Y, Barazzone C (2001) Role of CD40-CD40L in mouse severe malaria. Am J Pathol 159:733–742PubMedGoogle Scholar
  138. Pober JS, Cotran RS (1990) Cytokines and endothelial cell biology. Physiol Rev 70:427–451PubMedGoogle Scholar
  139. Pober JS, Cotran RS (1991) Immunologic interactions of T lymphocytes with vascular endothelium. Adv Immunol 50:261–302PubMedGoogle Scholar
  140. Polack B, Delolme F, Peyron F (1998) Protective role of platelets in chronic (BALB/c) and acute (CBA/J) Plasmodium berghei murine malaria. Haemostasis 27:278–285Google Scholar
  141. Polder TW, Jerusalem CR, Eling WMC (1983) Topographical distribution of the cerebral lesions in mice infected with Plasmodium berghei. Trop Med Parasitol 34:235–243Google Scholar
  142. Polder TW, Eling WMC, Curfs JHAJ, Jerusalem CR, Wijers-Rouw M (1992) Ultrastructural changes in the blood-brain barrier of mice infected with Plasmodium berghei. Acta Leidensia 60:31–46PubMedGoogle Scholar
  143. Potter S, Chaudhri G, Hansen A, Hunt NH (1999) Fas and perforin contribute to the pathogenesis of murine cerebral malaria. Redox Rep 4:333–335PubMedCrossRefGoogle Scholar
  144. Potter SM, Chaudhri G, Hansen AM, Hunt NH (1999) Fas and perforin contribute to the pathogenesis of murine cerebral malaria. Redox Rep 4:333–335PubMedCrossRefGoogle Scholar
  145. Pouvelle B, Buffet PA, Lepolard C, Scherf A, Gysin J (2000) Cytoadhesion of Plasmodium falciparum ring-stage-infected erythrocytes. Nature Med 6: 1264–1268PubMedGoogle Scholar
  146. Rajan AJ, Asensio VC, Campbell IL, Brosnan CF (2000) Experimental autoimmune encephalomyelitis on the SJL mouse: effect of γδ T cell depletion on chemokine and chemokine receptor expression in the central nervous system. J Immunol 164:2120–2130PubMedGoogle Scholar
  147. Rest JR, Wright DH (1979) Electron microscopy of cerebral malaria in golden hamsters (Mesocricetus auratus) infected with Plasmodium berghei. J Pathol 127:115–120PubMedCrossRefGoogle Scholar
  148. Rest JR (1982) Cerebral malaria in inbred mice. I. A new model and its pathology 2789. Trans R Soc Trop Med Hyg 76:410–415PubMedCrossRefGoogle Scholar
  149. Rest JR (1983) Pathogenesis of cerebral malaria in golden hamsters and inbred mice4592. Contrib Microbiol Immunol 7:139–146PubMedGoogle Scholar
  150. Rigdon RH, Fletcher DE (1944) Lesions of brain associated with malaria. Pathologic study on man and on experimental animals. Arch Neurol Psych 53:191–198Google Scholar
  151. Ringwald P, Peyron F, Vuillez JP, Touze JE, Le Bras J, Deloron P (1991) Levels of cytokines in plasma during Plasmodium falciparum malaria attacks. J Clin Microbiol 29:2076–2078PubMedGoogle Scholar
  152. Robert C, Peyrol S, Pouvelle B, Gay-Andrieu F, Gysin J (1996) Ultrastructural aspects of Plasmodium falciparum-infected erythrocyte adherence to endothelial cells of Saimiri brain microvasculature. Am J Trop Med Hyg 54:169–177PubMedGoogle Scholar
  153. Roberts DJ, Craig AG, Berendt AR, Pinches RA, Nash G, Marsh K, Newbold CI (1992) Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature 357:689–692PubMedCrossRefGoogle Scholar
  154. Roberts DJ, Pain A, Kai O, Kortok M, Marsh K (2000) Autoagglutination of malaria-infected red blood cells and malaria severity. Lancet 355:1427–1428PubMedCrossRefGoogle Scholar
  155. Rowe JA, Moulds JM, Newbold CI, Miller LH (1997) Plasmodium falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388:292–295PubMedCrossRefGoogle Scholar
  156. Rot A, von Andrian UH (2004) Chemokines in Innate and Adaptive Host Defense: Basic Chemokinese Grammar for Immune Cells. Annu Rev Immunol 22:891–928PubMedCrossRefGoogle Scholar
  157. Rudin W, Eugster HP, Bordmann G, Bonato J, Muller MT, Yamage M, Ryffel B (1997) Resistance to cerebral malaria in tumor necrosis factor-α/β-deficient mice is associated with a reduction of intercellular adhesion molecule-1 up-regulation and T helper type 1 response. Am J Pathol 150:257–266PubMedGoogle Scholar
  158. Rzepczyk CM, Anderson K, Stamatiou S, Townsend E, Allworth A, McCormack J, Whitby M (1997) γδ T cells: their immuno biology and role in malaria infections. Int J Parasitol 27:191–200PubMedGoogle Scholar
  159. Sanni LA, Jarra W, Li C, Langhorne J (2004) Cerebral edema and cerebral hemorrhages in interleukin-10-deficient mice infected with Plasmodium chabaudi. Infect Immun 72:3054–3058PubMedCrossRefGoogle Scholar
  160. Sanni LA, Thomas SR, Tattam BN, Moore DE, Chaudhri G, Stocker R, Hunt NH (1998) Dramatic changes in oxidative tryptophan metabolism along the kynurenine pathway in experimental cerebral and noncerebral malaria. Am J Pathol 152:611–619PubMedGoogle Scholar
  161. Sarfo BY, Singh S, Lillard JW, Quarshie A, Gyasi RK, Armah H, Adjei AA, Jolly P, Stiles JK (2004) The cerebral-malaria-associated expression of RANTES, CCR3 and CCR5 in post-mortem tissue samples. Ann Trop Med Parasitol 98:297–303PubMedCrossRefGoogle Scholar
  162. Schetters TPM, Curfs JHAJ, van Zon AAJC, Hermsen CC, Eling WMC (1989) Cerebral lesions in mice infected with Plasmodium berghei are the result of an immunopathological reaction. Trans R Soc Trop Med Hyg 83:103–104PubMedCrossRefGoogle Scholar
  163. Schmutzhard E, Gerstenbrand F (1984) Cerebral malaria in Tanzania. Its epidemiology, clinical symptoms and neurological long term sequelae in the light of 66 cases. Trans R Soc Trop Med Hyg 78:351–353PubMedCrossRefGoogle Scholar
  164. Schofield L, Hackett F (1993) Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. J Exp Med 177:145–53PubMedCrossRefGoogle Scholar
  165. Schofield L, Hewitt MC, Evans K, Siomos MA, Seeberger PH (2002) Synthetic GPI as a candidate anti-toxic vaccine in a model of malaria. Nature 418:785–789PubMedCrossRefGoogle Scholar
  166. Scragg IG, Hensmann M, Bate CA, Kwiatkowski D (1999) Early cytokine induction by Plasmodium falciparum is not a classical endotoxin-like process. Eur J Immunol 29:2636–2644PubMedCrossRefGoogle Scholar
  167. Sedgwick JD, Riminton DS, Cyster JG, Korner H (2000) Tumor necrosis factor: a master-regulator of leukocyte movement. Immunol Today 21:110–113PubMedCrossRefGoogle Scholar
  168. Senaldi G, Vesin C, Chang R, Grau GE, Piguet PF (1994) Role of polymorphonuclear neutrophil leukocytes and their integrin CD11a (LFA-1) in the pathogenesis of severe murine malaria. Infect Immun 62:1144–1149PubMedGoogle Scholar
  169. Senaldi G, Kremsner PG, Grau GE (1992) Nitric oxide and cerebral malaria. Lancet 340:1554PubMedCrossRefGoogle Scholar
  170. Sexton AC, Good RT, Hansen DS, D’Ombrain MC, Buckingham L, Simpson K, Schofield L (2004) Transcriptional profiling reveals suppressed erythropoiesis, up-regulated glycolysis, and interferon-associated responses in murine malaria. J Infect Dis 189:1245–1256PubMedCrossRefGoogle Scholar
  171. Sharma MC, Tripathi LM, Rastogi M, Maitra SC, Sagar P, Dutta GP, Pandey VC (1992) Aberrations in cerebral vascular functions due to Plasmodium yoelii nigeriensis infection in mice. Exp Mol Pathol 57:62–69PubMedCrossRefGoogle Scholar
  172. Sharma MR, Sharma MC, Tripathi LM, Pandey VC, Maitra SC (1994) Neuropathological studies on Plasmodium yoelii nigeriensis-induced malaria in mice. J Comp Pathol 110:313–317PubMedGoogle Scholar
  173. Silamut K, Phu NH, Whitty C, Turner GDH, Louwrier K, Mai NT, Simpson JA, Hien TT, White NJ (1999) A quantitative analysis of the microvascular sequestration of malaria parasites in the human brain. Am J Pathol 155:395–410PubMedGoogle Scholar
  174. Spitz S (1961) Pathology of tropical diseases. Saunders Co, PhiladelphiaGoogle Scholar
  175. Stach JL, Dufrenoy E, Roffi J, Bach MA (1986) T-cell subsets and natural killer activity in Plasmodium falciparum-infected children. Clin Immunol Immunopathol 38:129–134PubMedCrossRefGoogle Scholar
  176. Stager S, Alexander J, Kirby AC, Botto M, Rooijen NV, Smith DF, Brombacher F, Kaye PM (2003) Natural antibodies and complement are endogenous adjuvants for vaccine-induced CD8+ T-cell responses. Nature Med 9:1287–1292PubMedGoogle Scholar
  177. Stevenson MM, Riley EM (2004) Innate immunity to malaria. Nat Rev Immunol 4:169–180PubMedCrossRefGoogle Scholar
  178. Stoelcker B, Hehlgans T, Weigl K, Bluethmann H, Grau GE, Mannel DN (2002) Requirement for tumor necrosis factor receptor 2 expression on vascular cells to induce experimental cerebral malaria. Infect Immun 70:5857–5859PubMedCrossRefGoogle Scholar
  179. Sun G, Chang WL, Li J, Berney SM, Kimpel D, van der Heyde HC (2003) Inhibition of platelet adherence to brain microvasculature protects against severe Plasmodium berghei malaria. Infect Immun 71:6553–6561PubMedCrossRefGoogle Scholar
  180. Taniguchi M, Harada M, Kojo S, Nakayama T, Wakao H (2003) The regulatory role of Valpha14NKT cells in innate and acquired immunity. Annu Rev Immunol 21:483–513PubMedCrossRefGoogle Scholar
  181. Toro G, Roman G (1977) Cerebral malaria. A disseminated vasculomyelinopathy Pathophysiology of atypical malaria. J Assoc Physicians India 25:419–422Google Scholar
  182. Trowell HC, Davies JN, Dean RFA (1954) Kwashiorkor. Edward Arnold, LondonGoogle Scholar
  183. Troye-Blomberg M, Romero P, Patarroyo ME, Bjorkman A, Perlmann P (1984) Regulation of the immune response in Plasmodium falciparum malaria. III. Proliferative response to antigen in vitro and subset composition of T cells from patients with acute infection or from immune donors. Clin Exp Immunol 58:380–387PubMedGoogle Scholar
  184. Udomsangpetch R, Wahlin B, Carlson J, Berzins K, Torii M, Aikawa M, Perlmann P, Wahlgren M (1987) Plasmodium falciparum-infected erythrocytes form spontaneous erythrocytes rosettes. J Exp Med 169:1835–1840Google Scholar
  185. Van den Eertwegh AJ, Boersma WJ, Claassen E (1992) Immunological functions and in vivo cell-cell interactions of T cells in the spleen. Crit Rev Immunol 11: 337–380PubMedGoogle Scholar
  186. van der Heyde HC, Bauer PR, Sun G, Chang WL, Yin L, Fuseler J, Granger DN (2001) Assessing vascular permeability during experimental cerebral malaria by a radiolabeled monoclonal antibody technique. Infect Immun 69:3460–3465PubMedGoogle Scholar
  187. van Hensbroek MB, Palmer A, Onyiorah E, Schneider G, Jaffar S, Dolan G, Memming H, Frenkel J, Enwere G, Bennett S, Kwiatkowski D, Greenwood B (1996) The effect of a monoclonal antibody to tumor necrosis factor on survival from childhood cerebral malaria. J Infect Dis 174:1091–1097PubMedGoogle Scholar
  188. Van Kaer L, Ashton-Rickardt PG, Ploegh HL, Tonegawa S (1992) TAP1 mutant mice are deficient in antigen presentation, surface class I molecules, and CD4-CD8+ T cells 6481. Cell 71:1205–1214PubMedCrossRefGoogle Scholar
  189. Vincke IH, Lips MAH (1948) Un nouveau Plasmodium d’un rongeur sauvage du Congo, Plasmodium berghei n. sp. Ann Soc Belge Med Trop 28:97–105PubMedGoogle Scholar
  190. Wallach D, Varfolomeev EE, Malinin NL, Goltsev YV, Kovalenko AV, Boldin MP (1999) Tumor necrosis factor receptor and Fas signaling mechanisms. Annu Rev Immunol 17:331–367PubMedCrossRefGoogle Scholar
  191. Warrell DA, Molyneux ME, Beales PF (1990) Severe and complicated malaria. World Health Organization, Division of Control of Tropical Diseases. Trans R Soc Trop Med Hyg 84 Suppl 2:1–65Google Scholar
  192. Wassmer SC, Lepolard C, Traore B, Pouvelle B, Gysin J, Grau GE (2004) Platelets reorient Plasmodium falciparum-Infected erythrocyte cytoadhesion to activated endothelial cells. J Infect Dis 189:180–189PubMedCrossRefGoogle Scholar
  193. Weyrich AS, Prescott SM, Zimmerman GA (2002) Platelets, endothelial cells, inflammatory chemokines, and restenosis: complex signaling in the vascular play book. Circulation 106:1433–1435PubMedCrossRefGoogle Scholar
  194. White NJ, Ho M (1992) The pathophysiology of malaria. Adv Parasitol 31: 83–172PubMedCrossRefGoogle Scholar
  195. World health Organization (1990) Severe and complicated malaria. World Health Organization, Division of Control of Tropical Diseases. Trans R Soc Trop Med Hyg 84:1–65Google Scholar
  196. Wright DH (1968) The effect of neonatal thymectomy on the survival of golden hamsters infected with Plasmodium berghei. Br J Exp Pathol 49:379–384PubMedGoogle Scholar
  197. Wright DH, Masembe RM, Bazira ER (1971) The effect of antithymocyte serum on golden hamsters and rats infected with Plasmodium berghei. Br J Exp Pathol 52:465–477PubMedGoogle Scholar
  198. Yanez DM, Manning DD, Cooley AJ, Weidanz WP, van der Heyde HC (1996) Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J Immunol 157:1620–1624PubMedGoogle Scholar
  199. Yanez DM, Batchelder J, van der Heyde HC, Manning DD, Weidanz WP (1999) γδ T-Cell Function in Pathogenesis of Cerebral Malaria in Mice Infected with Plasmodium berghei ANKA. Infect Immun 67:446–448PubMedGoogle Scholar
  200. Yoeli M, Hargreaves BJ (1974) Brain capillary blockage produced by a virulent strain of rodent malaria. Science 184:572–573PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2005

Authors and Affiliations

  • C. Engwerda
    • 1
  • E. Belnoue
    • 2
  • A. C. Grüner
    • 2
  • L. Rénia
    • 2
  1. 1.Immunology and Infection LaboratoryQueensland Institute of Medical ResearchHerstonAustralia
  2. 2.Département d’ImmunologieInstitut Cochin, Hôpital CochinParisFrance

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